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The plant unique ESCRT component FREE1 regulates autophagosome closure

Author

Listed:
  • Yonglun Zeng

    (The Chinese University of Hong Kong)

  • Baiying Li

    (The Chinese University of Hong Kong)

  • Shuxian Huang

    (The Chinese University of Hong Kong)

  • Hongbo Li

    (South China Normal University)

  • Wenhan Cao

    (The Chinese University of Hong Kong)

  • Yixuan Chen

    (The Chinese University of Hong Kong)

  • Guoyong Liu

    (China Agricultural University)

  • Zhenping Li

    (The Chinese University of Hong Kong)

  • Chao Yang

    (South China Normal University)

  • Lei Feng

    (The Chinese University of Hong Kong)

  • Jiayang Gao

    (The Chinese University of Hong Kong)

  • Sze Wan Lo

    (The Chinese University of Hong Kong)

  • Jierui Zhao

    (Doctoral School of the University at Vienna and Medical University of Vienna
    Austrian Academy of Sciences, Vienna BioCenter)

  • Jinbo Shen

    (Zhejiang A&F University)

  • Yan Guo

    (China Agricultural University)

  • Caiji Gao

    (South China Normal University)

  • Yasin Dagdas

    (Austrian Academy of Sciences, Vienna BioCenter)

  • Liwen Jiang

    (The Chinese University of Hong Kong
    CUHK Shenzhen Research Institute
    The Chinese University of Hong Kong)

Abstract

The energy sensor AMP-activated protein kinase (AMPK) can activate autophagy when cellular energy production becomes compromised. However, the degree to which nutrient sensing impinges on the autophagosome closure remains unknown. Here, we provide the mechanism underlying a plant unique protein FREE1, upon autophagy-induced SnRK1α1-mediated phosphorylation, functions as a linkage between ATG conjugation system and ESCRT machinery to regulate the autophagosome closure upon nutrient deprivation. Using high-resolution microscopy, 3D-electron tomography, and protease protection assay, we showed that unclosed autophagosomes accumulated in free1 mutants. Proteomic, cellular and biochemical analysis revealed the mechanistic connection between FREE1 and the ATG conjugation system/ESCRT-III complex in regulating autophagosome closure. Mass spectrometry analysis showed that the evolutionary conserved plant energy sensor SnRK1α1 phosphorylates FREE1 and recruits it to the autophagosomes to promote closure. Mutagenesis of the phosphorylation site on FREE1 caused the autophagosome closure failure. Our findings unveil how cellular energy sensing pathways regulate autophagosome closure to maintain cellular homeostasis.

Suggested Citation

  • Yonglun Zeng & Baiying Li & Shuxian Huang & Hongbo Li & Wenhan Cao & Yixuan Chen & Guoyong Liu & Zhenping Li & Chao Yang & Lei Feng & Jiayang Gao & Sze Wan Lo & Jierui Zhao & Jinbo Shen & Yan Guo & Ca, 2023. "The plant unique ESCRT component FREE1 regulates autophagosome closure," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37185-6
    DOI: 10.1038/s41467-023-37185-6
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    References listed on IDEAS

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    1. Niccolò Mosesso & Niharika Savant Lerner & Tobias Bläske & Felix Groh & Shane Maguire & Marie Laura Niedermeier & Eliane Landwehr & Karin Vogel & Konstanze Meergans & Marie-Kristin Nagel & Malte Dresc, 2024. "Arabidopsis CaLB1 undergoes phase separation with the ESCRT protein ALIX and modulates autophagosome maturation," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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